XPACE4 is a localized pro-protein convertase required for mesoderm induction and the cleavage of specific TGFβ proteins in Xenopus development

Development

Volumn 132, Issue 3, 2005, Pages 591-602

  Birsoy, Bilge ^a   Berg, Linnea ^b   Williams, P Huw ^c   Smith, James C ^d   Wylie, Christopher C ^a   Christian, Jan L ^b   Heasman, Janet ^a  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Mesoderm induction; PACE4; TGF ; Vg1

Indexed keywords

LUCIFERASE; MESSENGER RNA; MYELOPID; PROTEIN XPACE4; SERINE PROTEINASE; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; ENZYME ASSAY; GASTRULATION; IN SITU HYBRIDIZATION; MESODERM; MITOCHONDRION; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SECRETION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; XENOPUS;

AMINO ACID SEQUENCE; ANIMALS; EMBRYO, NONMAMMALIAN; GASTRULA; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MESODERM; MOLECULAR SEQUENCE DATA; MOTHERS; OLIGONUCLEOTIDES, ANTISENSE; PARACRINE COMMUNICATION; PHENOTYPE; PROPROTEIN CONVERTASES; RNA, MESSENGER; SEQUENCE ALIGNMENT; SERINE ENDOPEPTIDASES; TRANSFORMING GROWTH FACTOR BETA; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 14044273683     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01599     Document Type: Article

References (48)

1. Akamatsu, T., Daikoku, S., Nagamune, H., Yoshida, S., Mori, K., Tsuji, A. and Matsuda, Y. (1997). Developmental expression of a novel Kexin family protease, PACE4E, in the rat olfactory system. Histochem. Cell Biol. 108, 95-103.
2. Apletalina, E., Appel, J., Lamango, N. S., Houghten, R. A. and Lindberg, I. (1998). Identification of inhibitors of prohormone convertases 1 and 2 using a peptide combinatorial library. J. Biol. Chem. 273, 26589-26595.
3. Beck, S., le Good, J. A., Guzman, M., Haim, N. B., Roy, K., Beermann, F. and Constam, D. B. (2002). Extraembryonic proteases regulate Nodal signalling during gastrulation. Nat. Cell Biol. 4 981-985.
4. Berthet, V., Rigot, V., Champion, S., Secchi, J., Fouchier, F., Marvaldi, J. and Luis, J. (2000). Role of endoproteolytic processing in the adhesive and signaling functions of alphavbeta5 integrin. J. Biol. Chem. 275, 33308-33313.
5. Clements, D., Friday, R. V. and Woodland, H. R. (1999). Mode of action of VegT in mesoderm and endoderm formation. Development 126, 4903-4911.
6. Constam, D. B. and Robertson, E. J. (1999). Regulation of bone morphogenetic protein activity by pro domains and proprotein convertases. J. Cell Biol. 144, 139-149.
7. Constam, D. B. and Robertson, E. J. (2000). SPC4/PACE4 regulates a TGFbeta signaling network during axis formation. Genes Dev. 14, 1146-1155.
8. Cui, Y., Jean, F., Thomas, G. and Christian, J. L. (1998). BMP-4 is proteolytically activated by furin and/or PC6 during vertebrate embryonic development. EMBO J. 17, 4735-4743.
9. Cui, Y., Hackenmiller, R., Berg, L., Jean, F., Nakayama, T., Thomas, G. and Christian, J. L. (2001). The activity and signaling range of mature BMP-4 is regulated by sequential cleavage at two sites within the prodomain of the precursor. Genes Dev. 15, 2797-2802.
10. Dale, L., Matthews, G., Tabe, L. and Colman, A. (1989). Developmental expression of the protein product of Vg1, a localized maternal mRNA in the frog Xenopus laevis. EMBO J. 8, 1057-1065.
11. Dale, L., Matthews, G. and Colman, A. (1993). Secretion and mesoderm-inducing activity of the TGF-beta-related domain of Xenopus Vg1. EMBO J. 12, 4471-4480.
12. De Cat, B., Muyldermans, S. Y., Coomans, C., Degeest, G., Vanderschueren, B., Creemers, J., Biemar, F., Peers, B. and David, G. (2003). Processing by proprotein convertases is required for glypican-3 modulation of cell survival, Wnt signaling, and gastrulation movements. J. Cell Biol. 163, 625-635.
13. Dohrmann, C. E., Kessler, D. S. and Melton, D. A. (1996). In duction of axial mesoderm by zDVR-1, the zebrafish orthologue of Xenopus Vg1. Dev. Biol. 175, 108-117.
14. Dubois, C. M., Laprise, M. H., Blanchette, F., Gentry, L. E. and Leduc, R. (1995). Processing of transforming growth factor beta 1 precursor by human furin convertase. J. Biol. Chem. 270, 10618-10624.
15. Eimon, P. M. and Harland, R. M. (2002). Effects of heterodimerization and proteolytic processing on Derriere and Nodal activity: implications for mesoderm induction in Xenopus. Development 129, 3089-3103.
16. Harland, R. M. (1991). In situ hybridization: an improved whole-mount method for Xenopus embryos. Methods Cell Biol. 36, 685-695.
17. Heasman, J., Quarmby, J. and Wylie, C. C. (1984). The mitochondrial cloud of Xenopus oocytes: the source of germinal granule material. Dev. Biol. 105, 458-469.
18. Henrich, S., Cameron, A., Bourenkov, G. P., Kiefersauer, R., Huber, R., Lindberg, I., Bode, W. and Than, M. E. (2003). The crystal structure of the proprotein processing proteinase furin explains its stringent specificity. Nat. Struct. Biol. 10, 520-526.
19. Huang, H. C., Murtaugh, L. C., Vize, P. D. and Whitman, M. (1995). Identification of a potential regulator of early transcriptional responses to mesoderm inducers in the frog embryo. EMBO J. 14, 5965-5973.
20. Jones, C. M., Kuehn, M. R., Hogan, B. L., Smith, J. C. and Wright, C. V. (1995). Nodal-related signals induce axial mesoderm and dorsalize mesoderm during gastrulation. Development 121, 3651-3662.
21. Kessler, D. S. and Melton, D. A. (1995). Induction of dorsal mesoderm by soluble, mature Vg1 protein. Development 121 2155-2164.
22. Kofron, M., Demel, T., Xanthos, J., Lohr, J., Sun, B., Sive, H., Osada, S., Wright, C., Wylie, C. and Heasman, J. (1999). Mesoderm induction in Xenopus is a zygotic event regulated by maternal VegT via TGFbeta growth factors. Development 126, 5759-5770.
23. Kofron, M., Klein, P., Zhang, F., Houston, D. W., Schaible, K., Wylie, C. and Heasman, J. (2001). The role of maternal axin in patterning the Xenopus embryo. Dev. Biol. 237, 183-201.
24. Kofron, M., Puck, H., Standley, H., Wylie, C., Old, R., Whitman, M. and Heasman, J. (2004). New roles for FoxH1 in patterning the early embryo. Development 131, 5065-5078.
25. Kramer, K. L. and Yost, H. J. (2002). Ectodermal syndecan-2 mediates left-right axis formation in migrating mesoderm as a cell-nonautonomous Vg1 cofactor. Dev. Cell 2, 115-124.
26. Leighton, M. and Kadler, K. E. (2003). Paired basic/Furin-like proprotein convertase cleavage of Pro-BMP-1 in the trans-Golgi network. J. Biol. Chem. 278, 18478-18484.
27. Lustig, K. D. and Kirschner, M. W. (1995). Use of an oocyte expression assay to reconstitute inductive signaling. Proc. Natl. Acad. Sci. USA 92, 6234-6238.
28. Mains, R. E., Berard, C. A., Denault, J. B., Zhou, A., Johnson, R. C. and Leduc, R. (1997). PACE4: a subtilisin-like endoprotease with unique properties. Biochem. J. 321, 587-593.
29. Melton, D. A. (1987). Translocation of a localized maternal mRNA to the vegetal pole of Xenopus oocytes. Nature 328 80-82.
30. Nieuwkoop, P. D. and Faber, J. (1967). Normal Table of Xenopus laevis (Daudin). Amsterdam, The Netherlands: North Holland Publishing Co.
31. Roebroek, A. J., Creemers, J. W., Pauli, I. G., Bogaert, T. and Van de Ven, W. J. (1993). Generation of structural and functional diversity in furin-like proteins in Drosophila melanogaster by alternative splicing of the Dfur1 gene. EMBO J. 12, 1853-1870.
32. Shah, S. B., Skromne, I., Hume, C. R., Kessler, D. S., Lee, K. J., Stern, C. D. and Dodd, J. (1997). Misexpression of chick Vg1 in the marginal zone induces primitive streak formation. Development 124, 5127-5138.
33. Stawowy, P., Kallisch, H., Veinot, J. P., Kilimnik, A., Prichett, W., Goetze, S., Seidah, N. G., Chretien, M., Fleck, E. and Graf, K. (2004). Endoproteolytic activation of alpha(v) integrin by proprotein convertase PC5 is required for vascular smooth muscle cell adhesion to vitronectin and integrin-dependent signaling. Circulation 109, 770-776.
34. Sun, B. I., Bush, S. M., Collins-Racie, L. A., LaVallie, E. R., DiBlasio-Smith, E. A., Wolfman, N. M., McCoy, J. M. and Sive, H. L. (1999). derriere: a TGF-beta family member required for posterior development in Xenopus. Development 126, 1467-1482.
35. Takahashi, S., Yokota, C., Takano, K., Tanegashima, K., Onuma, Y., Goto, J. and Asashima, M. (2000). Two novel nodal-related genes initiate early inductive events in Xenopus Nieuwkoop center. Development 127, 5319-5329.
36. Tannahill, D. and Melton, D. A. (1989). Localized synthesis of the Vg1 protein during early Xenopus development. Development 106, 775-785.
37. Taylor, N. A., van de Ven, W. J. and Creemers, J. W. (2003). Curbing activation: proprotein convertases in homeostasis and pathology. FASEB J. 17, 1215-1227.
38. Thomsen, G. H. and Melton, D. A. (1993). Processed Vg1 protein is an axial mesoderm inducer in Xenopus. Cell 74, 433-441.
39. Tsuji, A., Sakurai, K., Kiyokage, E., Yamazaki, T., Koide, S., Toida, K., Ishimura, K. and Matsuda, Y. (2003). Secretory proprotein convertases PACE4 and PC6A are heparin-binding proteins which are localized in the extracellular matrix. Potential role of PACE4 in the activation of proproteins in the extracellular matrix. Biochim. Biophys. Acta 1645, 95-104.
40. Weeks, D. L. and Melton, D. A. (1987). A maternal mRNA localized to the vegetal hemisphere in Xenopus eggs codes for a growth factor related to TGF-beta. Cell 51, 861-867.
41. Williams, P. H., Hagemann, A., Gonzalez-Gaitan, M. and Smith, J. C. (2004). Visualizing long-range movement of the morphogen xnr2 in the Xenopus embryo. Curr. Biol. 14, 1916-1923.
42. Xanthos, J. B., Kofron, M., Wylie, C. and Heasman, J. (2001). Maternal VegT is the initiator of a molecular network specifying endoderm in Xenopus laevis. Development 128, 167-180.
43. Xanthos, J. B., Kofron, M., Tao, Q., Schaible, K., Wylie, C. and Heasman, J. (2002). The roles of three signaling pathways in the formation and function of the Spemann Organizer. Development 129, 4027-4043.
44. Yana, I. and Weiss, S. J. (2000). Regulation of membrane type-1 matrix metalloproteinase activation by proprotein convertases. Mol. Biol. Cell 11, 2387-2401.
45. Yokota, C., Kofron, M., Zuck, M., Houston, D. W., Isaacs, H., Asashima, M., Wylie, C. C. and Heasman, J. (2003). A novel role for a nodal-related protein; Xnr-3 regulates convergent extension movements via the FGF receptor. Development 130, 2199-2212.
46. Zhang, J., Houston, D. W., King, M. L., Payne, C., Wylie, C. and Heasman, J. (1998). The role of maternal VegT in establishing the primary germ layers in Xenopus embryos. Cell 94, 515-524.
47. Zheng, M., Seidah, N. G. and Pintar, J. E. (1997). The developmental expression in the rat CNS and peripheral tissues of proteases PC5 and PACE4 mRNAs: comparison with other proprotein processing enzymes. Dev. Biol. 181, 268-283.
48. Zuck, M. V., Wylie, C. C. and Heasman, J. (1998). Maternal mRNAs in Xenopus embryos: an antisense approach. In A Comparative Methods Approach to the Study of Oocytes and Embryos (ed. J. D. Richter), pp. 341-354. Oxford, UK: Oxford University Press.